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Lepidostromatales, a new order of lichenized fungi (Basidiomycota, Agaricomycetes), with two new genera, Ertzia and Sulzbacheromyces, and one new species, Lepidostroma winklerianum

Abstract

We present a revised molecular phylogeny of higher Basidiomycota focusing on Lepidostromataceae based on the large subunit (28S) of the nuclear ribosomal rDNA (nuLSU), with additionl data from the translation elongation factor 1 alpha 1 (TEF1) and the RNA polymerase II second largest subunit (RPB2) genes. Our results suggest that Lepidostromataceae is best recognized in a separate order, Lepidostromatales ordo novum, within subclass Agaricomycetidae. Furthermore, the internal topology of Lepidostromataceae, correlating with thallus features, indicates that three genera, instead of a single genus, should be recognized. We therefore introduce the genera Ertzia genus novum and Sulzbacheromyces genus novum for Lepidostroma akagerae and L. caatingae, respectively. In addition, the new species L. winklerianum spec. nova is described for Mexican material previously identified as L. calocerum. The photobionts of Sulzbacheromyces and Lepidostroma were identified using molecular data of the large subunit of the ribulose 1,5-bisphosphate carboxylase/oxygenase (rbcL) gene, revealing a possibly undescribed genus in Trebouxiophyceae and the first report of lichenization for the genus Bracteacoccus in Chlorophyceae.

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References

  1. Ahmadjian V (1993) The lichen symbiosis. Wiley, New York

    Google Scholar 

  2. Alexopoulos CJ, Mims CW, Blackwell M (1996) Introductory mycology. Wiley, New York

    Google Scholar 

  3. Amend A, Samson R, Seifert K, Bruns T (2010) Deep sequencing reveals diverse and geographically structured assemblages of fungi in indoor dust. PNAS 107:13748–13753

    CAS  Article  PubMed  Google Scholar 

  4. Bruns TD, Szaro TM, Gardes M, Cullings KW, Pan J, Taylor DL, Li Y (1998) A sequence database for the identification of ectomycorrhizal fungi by sequence analysis. Mol Ecol 7:257–272

    CAS  Article  Google Scholar 

  5. Buée M, Reich M, Murat C, Nilsson RH, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456. doi:10.1111/j.1469-8137.2009.03003.x

    Article  PubMed  Google Scholar 

  6. Cannon PF, Kirk PM (2007) Fungal families of the world. CABI, Oxfordshire

    Google Scholar 

  7. Chaves JL, Lücking R, Sipman HJM, Umaña L, Navarro E (2004) A first assessment of the Ticolichen biodiversity inventory in Costa Rica: The genus Dictyonema (Polyporales: Atheliaceae). Bryologist 107:242–247. doi:10.1639/0007-2745

    Article  Google Scholar 

  8. Clémençon H, Emmet V, Emmet E (2004) Cytology and Plectology of the Hymenomycetes. Biblioth Mycol 199:1–488

    Google Scholar 

  9. Coppins BJ, James PW (1979) A British species of Dictyonema. Lichenologist 11:103–108. doi:10.1017/S002428297900013X

    Article  Google Scholar 

  10. Dai J, Liu X, Wang Y (2012) Genetic diversity and phylogeny of rhizobia isolated from Caragana microphylla growing in desert soil in Ningxia, China. Genet Mol Res 11:2683–2693. doi:10.4238/2012.June.25.5

    CAS  Article  PubMed  Google Scholar 

  11. Dal-Forno M, Lawrey JD, Sikaroodi M, Bhattarai S, Gillevet PM, Sulzbacher MA, Lücking R (2013) Starting from scratch: evolution of the lichen thallus in the basidiolichen Dictyonema (Agaricales: Hygrophoraceae). Fung Biol 117:584–598. doi:10.1016/j.funbio.2013.05.006

    CAS  Article  Google Scholar 

  12. Diederich P, Lawrey JD (2007) New lichenicolous, muscicolous, corticolous and lignicolous taxa of Burgoa s. l. and Marchandiomyces s. l. (anamorphic Basidiomycota), a new genus for Omphalina foliacea, and a catalogue and a key to the non-lichenized, bulbilliferous basidiomycetes. Mycol Prog 6:61–80. doi:10.1007/s11557-007-0523-3

    Article  Google Scholar 

  13. Ertz D, Lawrey JD, Sikaroodi M, Gillevet PM, Fischer E, Killmann D, Sérusiaux E (2008) A new lineage of lichenized basidiomycetes inferred from a two-gene phylogeny: The Lepidostromataceae with three species from the tropics. Am J Bot 95:1548–1556. doi:10.3732/ajb.0800232

    CAS  Article  PubMed  Google Scholar 

  14. Feuerer T, Hawksworth DL (2007) Biodiversity of lichens, including a world-wide analysis of checklist data based on Takhtajan’s floristic regions. Biodiv Cons 16:85–98. doi:10.1007/s10531-006-9142-6

    Article  Google Scholar 

  15. Fischer E, Ertz D, Killmann D, Sérusiaux E (2007) Two new species of Multiclavula (lichenized basidiomycetes) from savanna soils in Rwanda (East Africa). Bot J Linn Soc 155:457–465. doi:10.1111/j.1095-8339.2007.00717.x

    Article  Google Scholar 

  16. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  17. Hibbett DS, Binder M (2002) Evolution of complex fruiting body morphologies in homobasidiomycetes. Proc Roy Soc Lond B 269:1963–1969. doi:10.1098/rspb.2002.2123

    CAS  Article  Google Scholar 

  18. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch HT, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miądlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schußler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547. doi:10.1016/j.mycres.2007.03.004

    Article  PubMed  Google Scholar 

  19. Hodkinson BP (2012) An evolving phylogenetically based taxonomy of lichens and allied fungi. Opusc Philolich 11:4–10

    Google Scholar 

  20. Hodkinson BP, Uehling JK, Smith ME (2012a) Lepidostroma vilgalysii, a new basidiolichen from the new world. Mycol Prog 11:827–833. doi:10.1007/s11557-011-0800-z

    Article  Google Scholar 

  21. Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F (2012b) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161. doi:10.1111/j.1462-2920.2011.02560.x

    CAS  Article  PubMed  Google Scholar 

  22. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755. doi:10.1093/bioinformatics/17.8.754

    CAS  Article  PubMed  Google Scholar 

  23. Katoh K, Toh M (2005) MAFFT Version 5: Improvement in accuracy of multiple sequence alignment. Nucl Acids Res 33:511–518. doi:10.1093/nar/gki98

    CAS  Article  PubMed  Google Scholar 

  24. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CAB International, Wallingford

    Google Scholar 

  25. Kües U, Fischer R (2010) Growth, differentiation and sexuality (The Mycota). Springer, Berlin

    Google Scholar 

  26. Lawrey JD, Lücking R, Sipman HJM, Chaves JL, Redhead SA, Bungartz F, Sikaroodi M, Gillevet PM (2009) High concentration of basidiolichens in a single family of agaricoid mushrooms. Mycol Res 113:1154–1171. doi:10.1016/j.mycres.2009.07.016

    CAS  Article  PubMed  Google Scholar 

  27. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Pl Sci 31:1–46. doi:10.1080/07352689.2011.615705

    Article  Google Scholar 

  28. Lewis LA (1997) Diversity and phylogenetic placement of Bracteacoccus Tereg (Chlorophyceae, Chlorophyta) based on 18S ribosomal RNA gene sequence data. J Phycol 33:279–285. doi:10.1111/j.0022-3646.1997.00279.x

    CAS  Article  Google Scholar 

  29. Lücking R, Lawrey JD, Sikaroodi M, Gillevet PM, Chaves JL, Sipman HJM, Bungartz F (2009) Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. Am J Bot 96:1409–1418. doi:10.3732/ajb.0800258

    Article  PubMed  Google Scholar 

  30. Lücking R, Dal Forno M, Lawrey JD (2013) Last but not least: Witnessing the ‘birth’ of lichenization in the Basidiomycota. Mycologia (in review).

  31. Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179. doi:10.1111/j.1462-2920.2009.02099.x

    CAS  PubMed  Google Scholar 

  32. Mägdefrau K, Winkler S (1967) Lepidostroma terricolens n. g. n. sp., eine Basidiolichene der Sierra Nevada de Santa Marta (Kolumbien). Mitteil Inst Colombo-Alemán Invest Cient 1:11–17

    Google Scholar 

  33. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing inmicrofabricated high-density picolitre reactors. Nature 437:376–380. doi:10.1038/nature03959

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Matheny PB, Wang Z, Binder M, Curtis JM, Lim YW, Nilsson HR, Hughes KW, Hofstetter V, Ammirati JF, Schoch C, Langer E, Langer G, McLaughlin DJ, Wilson AW, Frøslev TG, Ge ZW, Yang ZL, Baroni TJ, Fischer M, Hosaka K, Matsuura K, Seidl MT, Vauras J, Hibbett DS (2007) Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Mol Phylogen Evol 43:430–451. doi:10.1016/j.ympev.2006.08.024

    CAS  Article  Google Scholar 

  35. McLaughlin DJ, McLaughlin EG, Lemke PA (eds) (2001) The Mycota: VIIA & B. Systematics and evolution. Springer, Berlin

    Google Scholar 

  36. Miller SL, Larsson E, Larsson KH, Verbeken A, Nuytinck J (2006) Perspectives in the new Russulales. Mycologia 98:960–970

    Google Scholar 

  37. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE): 1–8. New Orleans.

  38. Mueller GM, Bills GF, Foster MS (eds) (2004) Biodiversity of fungi. Inventory and monitoring methods. Elsevier Academic Press, New York

    Google Scholar 

  39. Nelsen MP, Lücking R, Umaña L, Trest MT, Will-Wolf S, Chaves JL, Gargas A (2007) Multiclavula ichthyiformis (Fungi: Basidiomycota: Cantharellales: Clavulinaceae), a remarkable new basidiolichen from Costa Rica. Am J Bot 94:1289–1296. doi:10.3732/ajb.94.8.1289

    Article  PubMed  Google Scholar 

  40. Nelsen MP, Lücking R, Grube M, Mbatchou JS, Muggia L, Rivas Plata E, Lumbsch HT (2009) Unraveling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Stud Mycol 64:135–144. doi:10.3114/sim.2009.64.07

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  41. Nilsson RH, Tedersoo L, Lindahl BD et al (2011) Towards standardization of the description and publication of next-generation sequencing datasets of fungal communities. New Phytol 191:314–318. doi:10.1111/j.1469-8137.2011.03755.x

    Article  Google Scholar 

  42. Oberwinkler F (1970) Die Gattungen der Basidiolichenen. Vortr Gesamtgeb Bot 4:139–169

    Google Scholar 

  43. Oberwinkler F (1984) Fungus-alga interactions in Basidiolichens. Beih Nova Hedwigia 79:739–774

    Google Scholar 

  44. Oberwinkler F (2001) Basidiolichens. In: Hock B (ed) The Mycota, vol IX, Fungal associations. Springer, New York, pp 211–225

    Google Scholar 

  45. Oberwinkler F (2012) Basidiolichens. In: Hock B (ed) The Mycota, vol IX, Fungal associations. Springer, New York, pp 341–362

    Google Scholar 

  46. Parmasto E (1978) The genus Dictyonema (‘Thelephorolichenes’). Nova Hedwigia 29:99–144

    Google Scholar 

  47. Penn O, Privman E, Landan G, Graur D, Pupko T (2010a) An alignment confidence score capturing robustness to guide-tree uncertainty. Mol Biol Evol 27:1759–1767. doi:10.1093/molbev/msq066

    CAS  Article  PubMed  Google Scholar 

  48. Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T (2010b) GUIDANCE: A web server for assessing alignment confidence scores. Nucl Acids Res 38:W23–W28. doi:10.1093/nar/gkq443

    CAS  Article  PubMed  Google Scholar 

  49. Petersen RH (1967) Notes on clavarioid fungi. VII. Redefinition of the Clavaria vernalis-C. mucida complex. Am Midland Nat 77:205–221

    Article  Google Scholar 

  50. Redhead SA, Lutzoni F, Moncalvo JM, Vilgalys R (2002) Phylogeny of agarics: Partial systematics solutions for core omphalinoid genera in the Agaricales (Euagarics). Mycotaxon 83:19–57

    Google Scholar 

  51. Rothberg JM, Leamon JH (2008) The development and impact of 454 sequencing. Nat Biotechnol 26:1117–1124. doi:10.1038/nbt1485

    CAS  Article  PubMed  Google Scholar 

  52. Schoch CL, Sung GH, López-Giráldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Matheny PB, Kauff F, Wang Z, Gueidan C, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Groenewald JZ, Arzanlou M, de Hoog GS, Crous PW, Hewitt D, Pfister DH, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh SO, Blackwell M, Hillis DM, Griffith GW, Castlebury LA, Rossman AY, Lumbsch HT, Lücking R, Büdel B, Rauhut A, Diederich P, Ertz D, Geiser DM, Hosaka K, Inderbitzin P, Kohlmeyer J, Volkmann-Kohlmeyer B, Mostert L, O’Donnell K, Sipman H, Rogers JD, Shoemaker RA, Sugiyama J, Summerbell RC, Untereiner W, Johnston PR, Stenroos S, Zuccaro A, Dyer PS, Crittenden PD, Cole MS, Hansen K, Trappe JM, Yahr R, Lutzoni F, Spatafora JW (2009) The Ascomycota tree of life: A phylum wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239. doi:10.1093/sysbio/syp020

    CAS  Article  PubMed  Google Scholar 

  53. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci U S A 103:12115–12120. doi:10.1073/pnas.0605127103

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  54. Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446

    CAS  Article  PubMed  Google Scholar 

  55. Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463. doi:10.1093/bioinformatics/bti191

    CAS  Article  PubMed  Google Scholar 

  56. Sulzbacher MA, Baseia IG, Lücking R, Parnmen S, Moncada B (2012) Unexpected discovery of a novel basidiolichen in the threatened Caatinga biome of northeastern Brazil. Bryologist 115:601–609. doi:10.1639/0007-2745-115.4.601

    Article  Google Scholar 

  57. Wallander H, Johansson U, Sterkenburg E, Durling MB, Lindahl B (2010) Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce. New Phytol 187:1124–1134. doi:10.1111/j.1469-8137.2010.03324.x

    CAS  Article  PubMed  Google Scholar 

  58. Weiss M, Oberwinkler F (2001) Phylogenetic relationships in Auriculariales and related groups—hypotheses derived from nuclear ribosomal DNA sequences. Mycol Res 105:403–415

    CAS  Article  Google Scholar 

  59. Yánez A, Dal-Forno M, Bungartz F, Lücking R, Lawrey JD (2012) A first assessment of Galapagos basidiolichens. Fung Div 52:225–244. doi:10.1007/s13225-011-0133-x

    Article  Google Scholar 

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Acknowledgments

Funding was provided to BPH through an Explorers Club Diversa Award, a Duke University Graduate International Research Travel Award, an American Bryological & Lichenological Society Student Travel Award, and a Sigma Xi Grant-In-Aid of Research. Partial financial support for RL was provided by grant DEB 0841405 from the National Science Foundation to George Mason University: “Phylogenetic Diversity of Mycobionts and Photobionts in the Cyanolichen Genus Dictyonema, with Emphasis on the Neotropics and the Galapagos Islands” (PI: J. Lawrey; Co-PIs: R. Lücking, P. Gillevet). Molecular sequence work by BM was partially supported by grant DEB 715660 from the National Science Foundation to The Field Museum: "Neotropical Epiphytic Microlichens–An Innovative Inventory of a Highly Diverse yet Little Known Group of Symbiotic Organisms" (PI R. Lücking).

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Correspondence to Brendan P. Hodkinson.

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Hodkinson, B.P., Moncada, B. & Lücking, R. Lepidostromatales, a new order of lichenized fungi (Basidiomycota, Agaricomycetes), with two new genera, Ertzia and Sulzbacheromyces, and one new species, Lepidostroma winklerianum . Fungal Diversity 64, 165–179 (2014). https://doi.org/10.1007/s13225-013-0267-0

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Keywords

  • Agaricales
  • Amylocorticiales
  • Atheliales
  • Auriculariales
  • BLAST
  • Boletales
  • Dictyonema
  • Diplosphaera
  • Gloeophyllales
  • Lichenomphalia
  • Marchandiomphalina
  • Multiclavula